Limnonectes phylax, Dehling & Neokleous & Das & Grafe & Min & Hertwig, 2025

Dehling, Maximilian, Neokleous, Dario N., Das, Indraneil, Grafe, Ulmar, Min, Pui Yong & Hertwig, Stefan T., 2025, Cryptic radiation within the tadpole-carrying Guardian Frogs from Borneo, Limnonectes palavanensis and L. finchi (Anura: Dicroglossidae), with the description of eight new species, Zootaxa 5650 (1), pp. 1-80 : 32-34

Limnonectes phylax sp. nov.

Rana microdisca palavanensis (nec Rana palavanensis Boulenger, 1894 )— Inger 1966: 222 (partim). Rana palavanensis (nec Rana palavanensis Boulenger, 1894 )— Inger & Voris 1988: 1060; Das 1995: 161. Limnonectes palavanensis (nec Rana palavanensis Boulenger, 1894 )— Das 2007: 53; Grafe & Keller 2009: 28; Grafe et al.

2010: 55; Goyes Vallejos & Ahmad Sah 2017: 608; Inger et al. 2017: 87 (partim); Goyes Vallejos et al. 2017: 1, 2018:

2473, 2019: 29.

Holotype. NMBE 1072362 , adult female, from Rhino Pool , Danum Valley Conservation Area, Sabah, Malaysia, collected on 2 March 2015 by S. T. Hertwig et al. ( Fig. 3F ).

Paratype. NMBE 1073856 , adult female, from Loop Walk (4.3742°, 115.43844°; 475 m), Merarap Hot Spring Lodge, Sarawak, Malaysia, collected on 1 March 2016 by J. Flury, A. Haas, S . T. Hertwig, Pui Y. M. and N. Reichen .

Referred material. NMBE 1064757 , tadpole, from Gunung Mulu National Park (100 m), Sarawak, Malaysia, collected on 11 March 2006 by I. Das,A. Haas and S . T. Hertwig . NMBE 1065198 , tadpole, from Tawau Hills National Park , Sabah, Malaysia, collected on 13 August 2007 by I. Das, C. Garratt, A. Haas and K. Hee . NMBE 1064089 , tadpoles, from Sungai Tawau (4.461083°, 117.920764°; 828 m), Tawau Hills National Park , Sabah, Malaysia, collected on 10 August 2007 . NMBE 1072710 , tadpoles, from Tembaling Waterfall (4.941332°, 117.807974°; 265 m), Danum Valley Conservation Area , Sabah, Malaysia, collected on 3 March 2015 by J. Flury, A. Haas and S . T. Hertwig . UBDM-GG010 , adult female ; UBDM-GG011 , GG011, adult male; both from Ashton Trail, towards Sungai Mata Ikan, near Kuala Belalong Field Studies Centre , Ulu Temburong National Park, Temburong, District, Brunei Darussalam, collected on 23 July 2012 by J. Goyes Vallejos. UBDM-GG012 , adult male, collected on 16 October 2014 ; UBDM-GG013 –GG014, two adult males , UBDM-GG015–017 , three adult females, all collected on 19 October and 19 November 2014 ; all from near Kuala Belalong Field Studies Centre, Ulu Temburong National Park, Temburong, District , Brunei Darussalam, collected by T. U. Grafe and J. Goyes Vallejos. SP 894, adult male, from Purulon Camp , Tenom District, Crocker Range, Sabah, Malaysia, collected on 23 June 1989 by “ R. F. Inger et al.”. SP 895, adult male, from “Mondolong” [= Mendolong ] , SFI, Sipitang, Sabah, Malaysia, collected on 2 August 1989 by “ R. F. Inger et al.”. SP 2242 (tag on specimen) or 2243 (jar label), adult male, from Long Pasia (4.40°, 115.72°; 1,000 m), Sipitang, Sabah, Malaysia, collected on 6 May 1998 by “Fred, Paul, et al.”. SP 2649, adult male, from Tawau Hills Park , Sabah, Malaysia, collected on 23 May 2000 by “Maklarin [Lakim], Alim [ Biun ] & Benedik ” .

Diagnosis. Limnonectes phylax sp. nov. belongs to the L. palavanensis species group, showing the typical characters of the group, including small size (SVL <40 mm); odontoid processes in lower jaw low and inconspicuous in both males and females; dorsum finely shagreened, with prominent longitudinal dorsolateral glandular ridges; interorbital distance equal to or larger than upper eyelid width; toes not fully webbed; and horseshoe-shaped dermal ridge in middle of dorsum posterior to arm insertion. The species differs from all other species of the group by a unique combination of morphological characters, including toe webbing moderately extensive; supratympanic fold strongly curved; pineal spot hardly discernible; vomer ridges long, narrowly separated from each other; postpalpebral ridge well developed, from upper eyelid to anterior level of pelvis; median ridge low from tip of snout to horseshoe-shaped ridge, much more conspicuous from horseshoe-shaped ridge to vent; lumbar ridge well developed; size relatively small with SVL of adult males 26.0– 28.5 mm, of adult females 30.1–34.5 mm. The species differs from all other species of the group by at least 6.6% in the sequence of the 16S barcoding gene. The advertisement call is a long rising trill, consisting of 21–39 notes, lasting 1.4– 2.2 s, at a dominant frequency of 1.4–2.1 kHz with a weak frequency modulation and an amplitude maximum in the first third of the call. The species occurs in lowland rainforest up to 830 m elevation.

Description of holotype. Adult female; SVL 32.0 mm; body moderately sturdy, widest at temporal region, slightly tapering to groin ( Fig. 3F ); head large (HL/SVL 0.35, HW/SVL 0.35), about as long as wide (HW/HL 1.01); snout long (SL/HL 0.47), subacuminate in dorsal view, rounded and slightly protruding in lateral profile, slightly wider than long (SL/EE 0.90); canthus rostralis moderately distinct between eye and nostril, almost straight-lined from eye to nostril in dorsal view; loreal region oblique; nostrils rounded, directed dorsolaterally; situated slightly closer to tip of snout and to eye (EN/NS 1.05), separated from each other by distance larger than distance between eye and nostril (NN/EN 1.39); eye directed anterolaterally, moderately protruding, very large (ED/HL 0.34), its diameter shorter than snout (ED/SL 0.72); interorbital distance about as wide as upper eyelid (IO/EW 1.06) and smaller than internarial distance (IO/NN 0.74); pineal spot hardly discernible, covered by skin, as small, low elevation posterior to level of anterior upper-eyelid edge; tympanum and its annulus visible, its posterodorsal edge in contact with supratympanic fold, its posteroventral edge covered by thick skin; tympanum separated from eye by two-fifth of its diameter (ET/TD 0.40); tympanum diameter smaller than eye diameter (TD/ED 0.62); upper jaw with dentition; odontoid processes in lower jaw low, inconspicuous; choanae small, rounded, located far anterolaterally at margins of roof of mouth, lateral third covered by palatal shelf of maxilla in ventral view; vomer processes bearing teeth, long, separated from choana by about half length of individual process, from each other by less than width of individual process, almost in contact medially ( Fig. 4F ); tongue short and broad, bilobed for about one-sixth of its length, free distally for about half its length; median lingual process absent.

Dorsal surfaces of head, trunk and limbs and lateral surfaces of trunk shagreened; enlarged tubercles sparsely scattered on upper eyelid and on dorsum; low, horseshoe-shaped dermal ridge in middle of back just behind level of arms; seven longitudinal dermal ridges running more or less parallelly to each other along back; dorsolateral ridge most prominent, from posterior end of upper eyelid to groin; postpalpebral ridge well developed, from upper eyelid to anterior level of pelvis; median ridge quite indistinct and very low from tip of snout to horseshoe-shaped ridge, continuing much more conspicuous from horseshoe-shaped ridge to vent; lumbar ridge well developed, from horseshoe ridge to vent, interrupted in posteriormost part; supratympanic fold thick and conspicuous, extending from posterior end of orbit, strongly curved, initially directed posterodorsally then turning sharply to arm insertion, straight-lined in its posterior fourth of length ( Fig. 5F ); ventral side of head, trunk and limbs smooth; transverse chest fold between arm insertions distinctly expressed; cloaca without dermal flap.

Forelimbs moderately sturdy; hand relatively small (HND/SVL 0.25); tips of fingers rounded, distinctly enlarged into disks; relative length of fingers: II = IV <I <III; subarticular tubercles rounded, well developed, numbering one on Fingers I and II, two on Fingers III and IV, proximal tubercles on Fingers III and IV larger and more prominent than distal ones; finger webbing absent; thenar tubercle oval, small, about two-fifth length of metacarpal of Finger I; inner and outer palmar tubercles fused proximally, forming roughly U-shaped, low tubercle on proximal third of metacarpals of Fingers II–IV.

Hindlimbs sturdy, very long (LEG /SVL 1.82); heel reaching distinctly beyond tip of snout when legs adpressed forwardly to body; tibiofibula long (TFL/SVL 0.58), slightly longer than thigh (TFL/THL 1.06); heels overlapping each other considerably when knees flexed and thighs held perpendicularly to median plane; foot slightly shorter than tibiofibula (FOT/TFL 0.91); relative length of toes: I <II <V <III <IV; toe tips rounded, enlarged into disks; subarticular tubercles numbering one on Toes I and II, two on Toes III and V, and three on Toe IV; pedal webbing formula I 1+/2 II 1+/2+ III 1+/2.5 IV 3-/1.25 V ( Fig. 6 ); narrow dermal ridge on preaxial side of Toe I and on postaxial side of Toe V from proximal end of metacarpus to disk; inner metatarsal tubercle prominent, elongated, about half length of metatarsus of Toe I; outer metatarsal tubercle absent.

Colouration. In life ( Fig. 7F ), dorsum light brown; horseshoe-shaped tubercle anteriorly coloured like dorsum with blackish brown posterior edge; dorsolateral fold with very narrow reddish line along medial edge and blackish brown lateral edge, black edge wider in posterior part; interorbital bar blackish brown with narrow cream anterior edge, lightening towards posterior edge to mid-brown, continued onto posterior part of upper eyelids; dorsal face of head anterior to interorbital bar as well as sides of snout greyish light brown; tympanic area bright yellowish, mottled with light brown; supratympanic fold and area above tympanum dark grey; flanks yellowish in anterior part, light grey in posterior part, with two dark brown spots in the middle; few small white dots at side of head, tympanic area and anterior part of flanks; arms pale yellow with few dark brown irregularly shaped spots; fingers dark brown with yellow spots; legs reddish light brown with greyish light brown crossbars; crossbars narrower and more frequent on thigh than on crus; ventral side of head, chest, arms, and legs bright yellow; abdomen pale yellow; dark brown speckling along postaxial side of lower arm and tarsus, and on preaxial and postaxial sides of thigh and crus; palmar side of hand and plantar side of foot dark brown.

In preserved state, dorsum of holotype grey overall with light brown tinge in anterior half of trunk and on crus. Reddish lines faded to brown; yellow colouration on arm faded to brownish grey; greyish brown crossbars on legs changed to light brown; upper eyelids with bluish tinge ( Fig. 3F ); ventral side of head, chest, and legs pale yellow; abdomen off white with bluish tinge in centre, pale orange on flanks; palmar side of hand and plantar side of feet light brown.

Variation. The paratypes match the holotype in general appearance. Males lack nuptial pads and have weak dermal folds parallel to posterior part of mandible on ventral side of head. The vocal sac aperture is slit-like, directed posterolaterally, situated at corner of mouth. SVL of adult males is 26.0– 28.5 mm, of adult females 30.1–34.5 mm ( Table 2). Inger & Voris (1988) recorded 25.2–28.2 mm SVL for males and 26.3–32.3 mm for females from Danum Valley.Pedal webbing variation is I 1 [63],1+ [25],1.25 [13] /2 II 1 [50],1+ [50] /2 [37],2+ [37],2.25 [13],2.5 [13] III 1 + [25],1.25 [37],1.5 [37] /2.5 [3 7],3- [63] IV2.75 [13],3- [87] /1 [37],1+ [25],1.25 [37] V ( Fig. 6 ) .

Bioacoustics. We have analyzed calls recorded at Camp 5, Gunung Mulu National Park (Sarawak, not collected), Ulu Temburong National Park ( Brunei, UBDM-GG011–14 ), Sepilok Forest Reserve ( Sabah , not collected) and Tawau Hills National Park ( Sabah , not collected). The call characteristics did not differ between the sites. The advertisement call of males (n=7) is a long rising trill, containing 21–39 notes and lasting 1.4– 2.2 s. Individual notes last 36–45 ms and are repeated at a rate of 15 notes/s. Dominant frequency is at 1.4–2.1 kHz, with a weak upward modulation from the beginning to the end or the call ( Fig. 11B ; Table 3). The amplitude initially increases rapidly, reaches its maximum within the first third of the call and subsequently slowly and weakly decreases until the end of the call ( Fig. 11B ). Females often call in response to the advertisement call of the male with very soft single-note squeaks or chirps, lasting on average 56.8 ± 9.0 ms, with a dominant frequency of 1,608 ± 67 Hz (Goyes Vallejos et al. 2017). Males use softer and shorter single-note courtship calls with an average duration of 309 ± 126 ms and an average dominant frequency of 1,752 ± 86 Hz in response to female calls (Goyes Vallejos et al. 2017). The call description as “a short, high-pitched trill” by Inger & Stuebing (1989) for specimens from Sabah roughly matches the call of L. phylax sp. nov..

Distribution. So far, the occurrence of species has been confirmed for a few locations between 100 and 830 m in eastern Sarawak (Gunung Mulu National Park, Merarap), Brunei Darussalam (Ulu Temburong National Park), and Sabah (Danum Valley, Tawau Hills National Park, Sepilok Forest Reserve) ( Fig. 8 ). We tentatively refer specimens from further locations in Sabah (Purulon, Sipitang) to the species. We expect the species to be widely distributed in lowland rainforests of northern Sarawak, Brunei, Sabah, as well as northeastern Kalimantan. The species occurs sympatrically with L. finchi in Sabah, and parapatrically with L. sarawakensis sp. nov. in the lowlands of Gunung Mulu National Park, Sarawak, where the species seem to be distributed in different forest types ( L. phylax sp. nov. in dipterocarp forest and karst forest, L. sarawakensis sp. nov. in alluvial forest); and with L. kinabaluensis sp. nov. in Tawau Hills National Park, Sabah, where the two species differ in elevational distribution with the latter occupying higher elevations ( Fig. 9 ).

Ecology. Eggs are deposited in moist leaf litter on top of dead leaves and guarded by the male ( Inger & Voris 1988). Clutches consist of 5– 21 eggs and tadpoles hatch at Gosner stage 24 or 25 9–11 days after oviposition ( Inger & Voris 1988; Goyes Vallejos et al. 2018). Males do not call during this time, nor do they care for more than one clutch at a time ( Goyes Vallejos et al. 2018). After hatching, the tadpoles crawl onto the male’s back and are transported to water bodies ( Inger & Voris 1988, Inger et al. 2017, Goyes Vallejos et al. 2018; Fig. 11 ). Observations of tadpole transport in the field indicate that all tadpoles from a clutch are retrieved at once and that the male stimulates synchronous hatching ( Goyes Vallejos et al. 2018). Adults of the species have been collected in the same forests blocks as L. finchi in Danum Valley ( Inger & Voris 1988). The species is preyed on by the Rough-backed Snake ( Xenodermus javanicus ) ( Goyes Vallejos & Ahmad Sah 2017).

Etymology. The species epithet derives from the Ancient Greek noun φύλαξ [phylax], meaning “guard” or “guardian”, and is used as a noun in apposition; in allusion to the egg-guarding behaviour of the males of the species.

Suggested English name. Smooth Guardian Frog.

Figures

FIGURE 3. Holotypes, lectotypes, and paratypes of the species of the Limnonectes palavanensis group (A–H) and L. finchi group (I & J): (A) Limnonectes palavanensis, lectotype (BMNH 1947.2.1.96, adult female); (B) L. gunungensis sp. nov., holotype (NMBE 1061576, adult female); (C) L. kinabaluensis sp. nov., holotype (NMBE 1075310, adult female); (D) L. nephophilus sp. nov., holotype (NMBE 1056394, adult male); (E) L. oreibates sp. nov., holotype (NMBE 1061519, adult female); (F) L. phylax sp. nov., holotype (NMBE 1072362, adult female); (G) L. sarawakensis sp. nov., holotype (NMBE 1057455, adult female); (H) L. suboliferus sp. nov., holotype (NMBE 1059945, adult female); (I) L. finchi, paratype (NMW 16961, adult male); (J) L. gyrinophorus sp. nov., holotype (NMBE 1075255, adult female). Scale bar represents 10 mm.

FIGURE 4. Relative size and position of teeth-bearing vomer ridges in (A) Limnonectes palavanensis—lectotype, BMNH 1947.2.1.96, adult female; (B) L. gunungensis sp. nov.—adult female, NMBE 1061576, holotype; (C) L. kinabaluensis sp. nov.—adult female, SP 1355; (D) L. nephophilus sp. nov.—adult male, NMBE 1073581, paratype; (E) L. oreibates sp. nov.— adult female, NMBE 1061519, holotype; (F) L. phylax sp. nov.—adult male, UBDM-GG012; (G) L. sarawakensis sp. nov.— adult female, NMBE 1057455, holotype; (H) L. suboliferus sp. nov.—adult male, NMBE 1059943, paratype; (I) L. finchi—adult female, NMBE 1072469; (J) L. gyrinophorus sp. nov.—adult female, NMBE 1075255, holotype.

FIGURE 5. Schematic drawings illustrating the shape of the supratympanic fold and the relative size and the position of the tympanum in the eight species of the L. palavanensis group: (A) Limnonectes palavanensis, (B) L. gunungensis sp. nov., (C) L. kinabaluensis sp. nov., (D) L. nephophilus sp. nov., (E) L. oreibates sp. nov., (F) L. phylax sp. nov., (G) L. sarawakensis sp. nov., (H) L. suboliferus sp. nov. (Drawings by J. M. Dehling).

FIGURE 6. Schematic drawings illustrating the extent of toe webbing in the eight species of the Limnonectes palavanensis group and the two species of the L. finchi group.Toes I to V are arranged from right to left in each drawing. Open circles represent terminal disks, filled circles represent subarticular tubercles. Solid lines represent the most common outline of webbing between toes, dotted lines represent the maximum or minimum extent due to variation between specimens.

FIGURE 7. Photographs of the species of the Limnonectes palavanensis group in life.A) Limnonectes palavanensis, adult male, Mt. Mantalingahan, Barangay Samarinana, Municipality of Brooke’s Point, Palawan Province, Palawan Island, Philippines (photo: R. Brown). (B) L. gunungensis sp. nov., paratype, adult male, Gunung Dulit, Sarawak, Malaysia (photo: S. T. Hertwig). (C) L. kinabaluensis sp. nov., holotype (NMBE 1075310), adult female, Silau-Silau Trail, Kinabalu National Park, Sabah, Malaysia (photo: S. Hertwig). (D) L. nephophilus sp. nov., holotype (NMBE 1056394), adult male, Camp 3, Gunung Mulu National Park, Sarawak, Malaysia (photo: J. M. Dehling). (E) L. oreibates sp. nov., paratype (UNIMAS P1186), adult male, Gunung Penrissen, Sarawak, Malaysia (photo: I. Das). (F) L. phylax sp. nov., adult male (not collected), Camp 5, Gunung Mulu National Park, Sarawak, Malaysia (photo: J. M. Dehling). (G) L. sarawakensis sp. nov., adult female (not collected), Headquarters, Gunung Mulu National Park, Sarawak, Malaysia (photo: J. M. Dehling). (H) L. suboliferus sp. nov., paratype (NMBE 1056615), adult male, Kubah National Park, Sarawak, Malaysia (photo: J. M. Dehling).

FIGURE 8. Collection localities of vouchers examined in the study of the different species of the L. palavanensis group and the L. finchi group in northern Borneo (Sarawak, Brunei, Sabah; main frame) and Palawan (inset). Respective localities are marked with a star (the exact type locality of L. palavanensis s. str. on Palawan is unknown). BK: Bukit Kana National Park, Sarawak; BP: Mt. Mantalingaha, Brooke’s Point, Palawan; DK: Deramakot, Sabah; DU: Gunung Dulit National Park, Sarawak; DV: Danum Valley Conservation Area, Sabah; GG: Gunung Gading National Park, Sarawak; GM: Gunung Mulu National Park, Sarawak; GT: Gunung Trusmadi, Sabah; KA: Kalabakan, Tawau District, Sabah; KB: Kuala Belalong Field Studies Centre, Ulu Temburong National Park, Brunei; KI: Kinabalu National Park, Headquarters, Sabah; KS: Kampung Sebako, Sarawak; KU: Kubah National Park, Matang Range, Sarawak; LH: Lambir Hills National Park, Sarawak; LP: Long Pasia, Sipitang, Sabah; LU: Long Unai, Sarawak; ME: Merarap Hot Spring Lodge, Sarawak; ML: Mendolong, Sipitang, Sabah; MR: Gunung Murud, Pulong Tau National Park, Sarawak; NT: Nanga Tekalit, Sarawak; PE: Gunung Penrissen, Sarawak; PM: Payeh Maga, Sarawak; PO: Kinabalu National Park, Poring, Sabah; PP: Barangay Irawan, Puerto Princesa, Palawan; PT: Pulong Tau National Park, Sarawak; PU: Purolon Camp, Crocker Range, Sabah; SP: Sepilok Forest Reserve, Sabah; SY: Kinabalu National Park, Sayap, Sabah; TW: Tawau Hills National Park. Map data © OpenStreetMap contributors.

FIGURE 9. Elevational distribution of the different species of Guardian Frogs, i.e. the L. finchi group, the L. palavanensis group and L. parvus.

FIGURE 11. Sound spectrograms (left) and corresponding waveforms (right) of typical advertisement calls or call series of (A) Limnonectes finchi, Danum Valley Conservation Area, Sabah, 400 m; (B) Limnonectes phylax sp. nov., Gunung Mulu National Park, Sarawak, 150 m; (C) L. sarawakensis sp. nov., Gunung Mulu National Park, Sarawak, 50 m; (D) L. nephophilus sp. nov., Gunung Mulu National Park, Sarawak, 1,300 m, (E) L. oreibates sp. nov., Gunung Penrissen, Sarawak, 1,000 m; (F) L. suboliferus sp. nov., Kubah National Park, Sarawak, 300 m; See Table 3 and respective species accounts for details.